Little evidence for release from herbivores as a driver of plant invasiveness from a multi‐species herbivore‐removal experiment

Enemy release is frequently posed as a main driver of invasiveness of alien species. However, an experimental multi‐species test examining performance and herbivory of invasive alien, non‐invasive alien and native plant species in the presence and absence of natural enemies is lacking. In a common garden experiment in Switzerland, we manipulated exposure of seven alien invasive, eight alien non‐invasive and fourteen native species from six taxonomic groups to natural enemies (invertebrate herbivores), by applying a pesticide treatment under two different nutrient levels. We assessed biomass production, herbivore damage and the major herbivore taxa on plants. Across all species, plants gained significantly greater biomass under pesticide treatment. However, invasive, non‐invasive and native species did not differ in their biomass response to pesticide treatment at either nutrient level. The proportion of leaves damaged on invasive species was significantly lower compared to native species, but not when compared to non‐invasive species. However, the difference was lost when plant size was accounted for. There were no differences between invasive, non‐invasive and native species in herbivore abundance. Our study offers little support for invertebrate herbivore release as a driver of plant invasiveness, but suggests that future enemy release studies should account for differences in plant size among species.     

Comparisons of arthropod assemblages on an invasive and native trees: abundance,diversity and damage

The success of exotic plants may be due to lower herbivore loads than those on native plants (Enemies Release Hypothesis). Predictions of this hypothesis include lower herbivore abundances, diversity, and damage on introduced plant species compared to native ones. Greater density or diversity of predators and parasitoids on exotic versus native plants may also reduce regulation of exotic plants by herbivores. To test these predictions, we measured arthropod abundance, arthropod diversity, and foliar damage on invasive Chinese tallow tree (Triadica sebifera) and three native tree species: silver maple (Acer saccharinum), sycamore (Platanus occidentalis), and sweetgum (Liquidambar styraciflua). Arthropod samples were collected with canopy sweep nets from six 20 year old monoculture plots of each species at a southeast Texas site. A total of 2,700 individuals and 285 species of arthropods were caught. Overall, the species richness and abundance of arthropods on tallow tree were similar to the natives. But, ordination (NMS) showed community composition differed on tallow tree compared to all three native trees. It supported an arthropod community that had relatively lower herbivore abundance but relatively more predator species compared to the native species examined. Leaves were collected to determine damage. Tallow tree experienced less mining damage than native trees. The results of this study supported the Enemies Release Hypothesis predictions that tallow tree would have low herbivore loads which may contribute to its invasive success. Moreover, a shift in the arthropod community to fewer herbivores without a reduction in predators may further limit regulation of this exotic species by herbivores in its introduced range.     

Invasive Eupatorium adenophorum suffers lower enemy impact on carbon assimilation than native congeners

Enemy release hypothesis predicts that alien plants that escape from their natural enemies suffer lower enemy regulation in their introduced ranges than in native ranges. An extension of this theory suggests that if enemy release plays a crucial role in invasive success, then in the introduced range, invasive plants should also suffer lower local enemy impact than native residents (local enemy release hypothesis, LERH). In order to test LERH, we compared invasive Eupatorium adenophorum with two native congeners (E. heterophyllum and E. japonicum) in terms of damage by leaf enemies at two natural field sites and two manipulated sites. We also determined enemy impact on carbon assimilation at two manipulated sites. In each site, E. adenophorum was only damaged by herbivores, while in native congeners, leaf scabs or (and) leaf rolls was found in addition to herbivory damage. In both manipulated sites, the total enemy impact on carbon assimilation was lower for E. adenophorum than for native congeners; this observation was consistent with LERH. The results of this study indicate that a short co-existence time with generalist enemies (behavior constraint) might be the main contributor to the lower enemy impact on E. adenophorum.     

Herbivory on invasive exotic plants and their non-invasive relatives

The Enemy Release Hypothesis links exotic plant success to escape from enemies such as herbivores and pathogens. Recent work has shown that exotic plants that more fully escape herbivores and pathogens are more likely to become highly invasive, compared to plants with higher enemy loads in their novel ranges. We predicted that highly invasive plants from the Asteraceae and the Brassicaceae would be less acceptable, in laboratory no-choice feeding trials, to the generalist herbivore the American grasshopper, Schistocerca americana. We also compared herbivory on invasive and non-invasive plants from the genus Centaurea in no-choice feeding trials using the red-legged grasshopper Melanoplus femurrubrum and in a common garden in the field. In accordance with our predictions, highly invasive plants were fed on less by grasshoppers in the laboratory. They also received less damage in the field, suggesting that they contain feeding deterrents that render them less acceptable to generalist herbivores than non-invasive plants.     

Phytophagous Insects on Native and Non-Native Host Plants: Combining the Community Approach and the Biogeographical Approach

During the past centuries, humans have introduced many plant species in areas where they do not naturally occur. Some of these species establish populations and in some cases become invasive, causing economic and ecological damage. Which factors determine the success of non-native plants is still incompletely understood, but the absence of natural enemies in the invaded area (Enemy Release Hypothesis; ERH) is one of the most popular explanations. One of the predictions of the ERH, a reduced herbivore load on non-native plants compared with native ones, has been repeatedly tested. However, many studies have either used a community approach (sampling from native and non-native species in the same community) or a biogeographical approach (sampling from the same plant species in areas where it is native and where it is non-native). Either method can sometimes lead to inconclusive results. To resolve this, we here add to the small number of studies that combine both approaches. We do so in a single study of insect herbivory on 47 woody plant species (trees, shrubs, and vines) in the Netherlands and Japan. We find higher herbivore diversity, higher herbivore load and more herbivory on native plants than on non-native plants, generating support for the enemy release hypothesis.     

Comparison of damage to native and exotic tallgrass prairie plants by natural enemies

We surveyed the prevalence and amount of leaf damage related to herbivory and pathogens on 12 pairs of exotic (invasive and noninvasive) and ecologically similar native plant species in tallgrass prairie to examine whether patterns of damage match predictions from the enemy release hypothesis. We also assessed whether natural enemy impacts differed in response to key environmental factors in tallgrass prairie by surveying the prevalence of rust on the dominant C₄ grass, Andropogon gerardii, and its congeneric invasive exotic C₄ grass, A. bladhii, in response to fire and nitrogen fertilization treatments. Overall, we found that the native species sustain 56.4% more overall leaf damage and 83.6% more herbivore-related leaf damage when compared to the exotic species. Moreover, we found that the invasive exotic species sustained less damage from enemies relative to their corresponding native species than the noninvasive exotic species. Finally, we found that burning and nitrogen fertilization both significantly increased the prevalence of rust fungi in the native grass, while rust fungi rarely occurred on the exotic grass. These results indicate that reduced damage from enemies may in part explain the successful naturalization of exotic species and the spread of invasive exotic species in tallgrass prairie.     

Testing the enemy release hypothesis: a review and meta-analysis

One of the most cited hypotheses explaining the inordinate success of a small proportion of introduced plants that become pests is the ‘natural enemies hypothesis’. This states that invasive introduced plants spread rapidly because they are liberated from their co-evolved natural enemies. This hypothesis had not been properly tested until recently. Previous reviews on this topic have been narrative and vote counting in nature. In this review, we carried out quantitative synthesis and meta-analysis using existing literature on plants and their herbivores to test the different components of the enemy release hypothesis. We found supporting evidence in that (1) insect herbivore fauna richness is significantly greater in the native than introduced ranges, and the reduction is skewed disproportionally towards specialists and insects feeding on reproductive parts; and (2) herbivore damage levels are greater on native plants than on introduced invasive congeners. However, herbivore damage levels are only marginally greater for plants in native than in introduced ranges, probably due to the small numbers of this type of study. Studies quantifying herbivore impacts on plant population dynamics are too scarce to make conclusions for either comparison of plants in native vs introduced ranges or of co-occurring native and introduced congeners. For future research, we advocate that more than two-way comparisons between plants in native and introduced ranges, or native and introduced congeners are needed. In addition, the use of herbivore exclusions to quantify the impacts of herbivory on complete sets of population vital rates of native vs introduced species are highly desirable. Furthermore, three-way comparisons among congeners of native plants, introduced invasive, and introduced non-invasive plants can also shed light on the importance of enemy release. Finally, simultaneously testing the enemy release hypothesis and other competing hypotheses will provide significant insights into the mechanisms governing the undesirable success of invasive species.     

Release from herbivory does not confer invasion success for Eugenia uniflora in Florida

One of the most commonly cited hypotheses explaining invasion success is the enemy release hypothesis (ERH), which maintains that populations are regulated by coevolved natural enemies where they are native but are relieved of this pressure in the new range. However, the role of resident enemies in plant invasion remains unresolved. We conducted a field experiment to test predictions of the ERH empirically using a system of native, introduced invasive, and introduced non-invasive Eugenia congeners in south Florida. Such experiments are rarely undertaken but are particularly informative in tests of the ERH, as they simultaneously identify factors allowing invasive species to replace natives and traits determining why most introduced species are unsuccessful invaders. We excluded insect herbivores from seedlings of Eugenia congeners where the native and invasive Eugenia co-occur, and compared how herbivore exclusion affected foliar damage, growth, and survival. We found no evidence to support the ERH in this system, instead finding that the invasive E. uniflora sustained significantly more damage than the native and introduced species. Interestingly, E. uniflora performed better than, or as well as, its congeners in terms of growth and survival, in spite of higher damage incidence. Further, although herbivore exclusion positively influenced Eugenia seedling survival, there were few differences among species and no patterns in regard to invasion status or origin. We conclude that the ability of E. uniflora to outperform its native and introduced non-invasive congeners, and not release from insect herbivores, contributes to its success as an invader in Florida.     

Competitive ability,not tolerance,may explain success of invasive plants over natives

When entering a new community, introduced species leave behind members of their native community while simultaneously forming novel biotic interactions. Escape from enemies during the process of introduction has long been hypothesized to drive the increased performance of invasive species. However, recent studies and quantitative syntheses find that invaders often receive similar, or even more, damage from enemies than do native species. Therefore, invasives may be those more tolerant to enemy damage, or those able to maintain competitive ability in light of enemy damage. Here, we investigate whether tolerance and competitive ability could contribute to invasive plant success. We determined whether invasive plants were more competitive than native or noninvasive exotic species in both the presence and absence of simulated herbivory. We found competition and herbivory additively reduced individual performance, and affected the performance of native, invasive, and noninvasive exotic species’ to the same degree. However, invasives exerted stronger competitive effects on an abundant native species (Elymus canadensis) in both the presence and absence of herbivory. Therefore, while invasive species responded similarly to competition and simulated herbivory, their competitive effects on natives may contribute to their success in their introduced range.     

Invading from the garden? A comparison of leaf herbivory for exotic and native plants in natural and ornamental settings

Abstract The enemies release hypothesis proposes that exotic species can become invasive by escaping from predators and parasites in their novel environment. Agrawal et al. (Enemy release? An experiment with congeneric plant pairs and diverse above‐ and below‐ground enemies. Ecology, 86, 2979–2989) proposed that areas or times in which damage to introduced species is low provide opportunities for the invasion of native habitat. We tested whether ornamental settings may provide areas with low levels of herbivory for trees and shrubs, potentially facilitating invasion success. First, we compared levels of leaf herbivory among native and exotic species in ornamental and natural settings in Cincinnati, Ohio, United States. In the second study, we compared levels of herbivory for invasive and noninvasive exotic species between natural and ornamental settings. We found lower levels of leaf damage for exotic species than for native species; however, we found no differences in the amount of leaf damage suffered in ornamental or natural settings. Our results do not provide any evidence that ornamental settings afford additional release from herbivory for exotic plant species.     

Comparison of invertebrate herbivores on native and non‐native Senecio species: Implications for the enemy release hypothesis

The enemy release hypothesis posits that non‐native plant species may gain a competitive advantage over their native counterparts because they are liberated from co‐evolved natural enemies from their native area. The phylogenetic relationship between a non‐native plant and the native community may be important for understanding the success of some non‐native plants, because host switching by insect herbivores is more likely to occur between closely related species. We tested the enemy release hypothesis by comparing leaf damage and herbivorous insect assemblages on the invasive species Senecio madagascariensis Poir. to that on nine congeneric species, of which five are native to the study area, and four are non‐native but considered non‐invasive. Non‐native species had less leaf damage than natives overall, but we found no significant differences in the abundance, richness and Shannon diversity of herbivores between native and non‐native Senecio L. species. The herbivore assemblage and percentage abundance of herbivore guilds differed among all Senecio species, but patterns were not related to whether the species was native or not. Species‐level differences indicate that S. madagascariensis may have a greater proportion of generalist insect damage (represented by phytophagous leaf chewers) than the other Senecio species. Within a plant genus, escape from natural enemies may not be a sufficient explanation for why some non‐native species become more invasive than others.     

Response to enemies in the invasive plant Lythrum salicaria is genetically determined

Background and Aims

The enemy release hypothesis assumes that invasive plants lose their co-evolved natural enemies during introduction into the new range. This study tested, as proposed by the evolution of increased competitive ability (EICA) hypothesis, whether escape from enemies results in a decrease in defence ability in plants from the invaded range. Two straightforward aspects of the EICA are examined: (1) if invasives have lost their enemies and their defence, they should be more negatively affected by their full natural pre-invasion herbivore spectrum than their native conspecifics; and (2) the genetic basis of evolutionary change in response to enemy release in the invasive range has not been taken sufficiently into account.

Methods

Lythrum salicaria (purple loosestrife) from several populations in its native (Europe) and invasive range (North America) was exposed to all above-ground herbivores in replicated natural populations in the native range. The experiment was performed both with plants raised from field-collected seeds as well as with offspring of these where maternal effects were removed.

Key Results

Absolute and relative leaf damage was higher for introduced than for native plants. Despite having smaller height growth rate, invasive plants attained a much larger final size than natives irrespective of damage, indicating large tolerance rather than effective defence. Origin effects on response to herbivory and growth were stronger in second-generation plants, suggesting that invasive potential through enemy release has a genetic basis.

Conclusions

The findings support two predictions of the EICA hypothesis – a genetically determined difference between native and invasive plants in plant vigour and response to enemies – and point to the importance of experiments that control for maternal effects and include the entire spectrum of native range enemies.     

Does time since introduction influence enemy release of an invasive weed?

Release from natural enemies is considered to potentially play an important role in the initial establishment and success of introduced plants. With time, the species richness of herbivores using non-native plants may increase [species-time relationship (STR)]. We investigated whether enemy release may be limited to the early stages of invasion. Substituting space for time, we sampled invertebrates and measured leaf damage on the invasive species Senecio madagascariensis Poir. at multiple sites, north and south of the introduction site. Invertebrate communities were collected from plants in the field, and reared from collected plant tissue. We also sampled invertebrates and damage on the native congener Senecio pinnatifolius var. pinnatifolius A. Rich. This species served as a control to account for environmental factors that may vary along the latitudinal gradient and as a comparison for evaluating the enemy release hypothesis (ERH). In contrast to predictions of the ERH, greater damage and herbivore abundances and richness were found on the introduced species S. madagascariensis than on the native S. pinnatifolius. Supporting the STR, total invertebrates (including herbivores) decreased in abundance, richness and Shannon diversity from the point of introduction to the invasion fronts of S. madagascariensis. Leaf damage showed the opposite trend, with highest damage levels at the invasion fronts. Reared herbivore loads (as opposed to external collections) were greater on the invader at the point of introduction than on sites further from this region. These results suggest there is a complex relationship between the invader and invertebrate community response over time. S. madagascariensis may be undergoing rapid changes at its invasion fronts in response to environmental and herbivore pressure.     

Variation in Herbivore Damage to Invasive and Native Woody Plant Species in Open Forest Vegetation on Mahé, Seychelles

Enemy release of introduced plants and variation in herbivore pressure in relation to community diversity are presently discussed as factors that affect plant species invasiveness or habitat invasibility. So far few data are available on this topic and the results are inconclusive. We compared leaf herbivory between native and invasive woody plants on Mahé, the main island of the tropical Seychelles. We further investigated variation in leaf herbivory on three abundant invasive species along an altitudinal gradient (50–550 m a.s.l.). The median percentage of leaves affected by herbivores was significantly higher in native species (50%) than in invasive species (27%). In addition, the species suffering from the highest leaf area loss were native to the Seychelles. These results are consistent with the enemy release hypothesis (ERH). While the invasive species showed significant and mostly consistent variation in the amount of leaf damage between sites, this variation was not related to general altitudinal trends in diversity but rather to local variation in habitat structure and diversity. Our results indicate that in the Seychelles invasive woody plants profit from herbivore release relative to the native species and that the amount of herbivory, and therefore its effect on species invasiveness or habitat invasibility, may be dependent on local community structure and composition.     

外来入侵杂草的生物防治及生防因子对本地非目标种的影响

随着生物入侵所引起的生态及经济问题日益严重,对有害入侵生物的防治问题也备受人们关注。生物防治因具有持续、高效、安全等优点,已成为防治有害入侵生物的重要方法。传统生防是防治有害入侵杂草的一种重要方法。在简单介绍生物防治的基础上,重点阐述了传统生物防治的理论基础——天敌逃逸假说,生防因子对外来人侵种的影响及其对本地非目标种的直接和间接效应,并针对这些问题,对我国开展生物防治工作提出几点建议。     

Differences in growth and herbivory damage of native and invasive kudzu (Peuraria montana var. lobata) populations grown in the native range

The invasion success of exotic plants is often attributed to escape from natural enemies in their introduced ranges and subsequent evolutionary change in resource allocation from defense to growth and reproduction. We tested this idea by comparing resistance, tolerance, and growth between native (China) and invasive (US) populations of kudzu (Peuraria montana var. lobata) exposed to natural herbivores in the native range. The percentage of foliar damage was much higher in invasive populations than in native populations, indicating that plants from invasive populations had lower resistance to herbivory. Regression of total mass on percentage of foliar damage showed no significant differences in tolerance to herbivory between native and invasive populations. However, stem diameter and mass were significantly greater in invasive populations than in native populations. Our results may suggest geographic variation in herbivory damage and plant growth among kudzu native and invasive populations, but the role of herbivores influencing kudzu invasion requires further investigation.     

Interactions between resource availability and enemy release in plant invasion

Understanding why some exotic species become invasive is essential to controlling their populations. This review discusses the possibility that two mechanisms of invasion, release from natural enemies and increased resource availability, may interact. When plants invade new continents, they leave many herbivores and pathogens behind. Species most regulated by enemies in their native range have the most potential for enemy release, and enemy regulation may be strongest for high-resource species. High resource availability is associated with low defence investment, high nutritional value, high enemy damage and consequently strong enemy regulation. Therefore, invasive plant species adapted to high resource availability may also gain most from enemy release. Strong release of high-resource species would predict that: (i) both enemy release and resources may underlie plant invasion, leading to potential interactions among control measures; (ii) increases in resource availability due to disturbance or eutrophication may increase the advantage of exotic over native species; (iii) exotic species will tend to have high-resource traits relative to coexisting native species; and (iv) although high-resource plants may experience strong enemy release in ecological time, well-defended low-resource plants may have stronger evolutionary responses to the absence of enemies.     

Tolerance and resistance of invasive and native Eupatorium species to generalist herbivore insects

Invasive plants are exotic species that escape control by native specialist enemies. However, exotic plants may still be attacked by locally occurring generalist enemies, which can influence the dynamics of biological invasions. If invasive plants have greater defensive (resistance and tolerance) capabilities than indigenous plants, they may experience less damage from native herbivores. In the present study, we tested this prediction using the invasive plant Eupatorium adenophorum and two native congeners under simulated defoliation and generalist herbivore insect (Helicoverpa armigera and Spodoptera litura) treatments. E. adenophorum was less susceptible and compensated more quickly to damages in biomass production from both treatments compared to its two congeners, exhibiting greater herbivore tolerance. This strong tolerance to damage was associated with greater resource allocation to aboveground structures, leading to a higher leaf area ratio and a lower root: crown mass ratio than those of its native congeners. E. adenophorum also displayed a higher resistance index (which integrates acid detergent fiber, nitrogen content, carbon/nitrogen ratio, leaf mass per area, toughness, and trichome density) than its two congeners. Thus, H. armigera and S. litura performed poorly on E. adenophorum, with less leaf damage, a lengthened insect developmental duration, and decreased pupating: molting ratios compared to those of the native congeners. Strong tolerance and resistance traits may facilitate the successful invasion of E. adenophorum in China and may decrease the efficacy of leaf-feeding biocontrol agents. Our results highlight both the need for further research on defensive traits and their role in the invasiveness and biological control of exotic plants, and suggest that biocontrol of E. adenophorum in China would require damage to the plant far in excess of current levels.     

Does enemy release matter for invasive plants? evidence from a comparison of insect herbivore damage among invasive,non-invasive and native congeners

One of the most popular single-factor hypotheses that have been proposed to explain the naturalization and spread of introduced species is the enemy release hypothesis (ERH). One ramification of the ERH is that invasive plants sustain less herbivore damage than their native counterparts in the invaded range. However, introduced plants, invasive or not, may experience less herbivore damage than the natives. Therefore, to test the role of natural enemies in the success of invasive plants, studies should include both invasive as well as non-invasive introduced species. In this study, we employed a novel three-way comparison, in which we compared herbivore damage among native, introduced invasive, and introduced non-invasive Eugenia (Myrtaceae) in South Florida. We found that introduced Eugenia, both invasive and non-invasive, sustained less herbivore damage, especially damage by oligophagous and endophagous insects, than native Eugenia. However, the difference in insect damage between introduced invasive and introduced non-invasive Eugenia was not significant. Escape from herbivores may not account for the spread of invasive Eugenia. We would not have been able to draw this conclusion without inclusion of the non-invasive Eugenia species in the study.     

Bird predation enhances tree seedling resistance to insect herbivores in contrasting forest habitats

According to the associational resistance hypothesis, neighbouring plants are expected to influence both the insect herbivore communities and their natural enemies. However, this has rarely been tested for the effects of canopy trees on herbivory of seedlings. One possible mechanism responsible for associational resistance is the indirect impact of natural enemies on insect herbivory, such as insectivorous birds. But it remains unclear to what extent such trophic cascades are influenced by the composition of plant associations (i.e. identity of ‘associated’ plants). Here, we compared the effect of bird exclusion on insect leaf damage for seedlings of three broadleaved tree species in three different forest habitats. Exclusion of insectivorous birds affected insect herbivory in a species-specific manner: leaf damage increased on Betula pendula seedlings whereas bird exclusion had no effect for two oaks (Quercus robur and Q. ilex). Forest habitat influenced both the extent of insect herbivory and the effect of bird exclusion. Broadleaved seedlings had lower overall leaf damage within pine plantations than within broadleaved stands, consistent with the resource concentration hypothesis. The indirect effect of bird exclusion on leaf damage was only significant in pine plantations, but not in exotic and native broadleaved woodlands. Our results support the enemies hypothesis, which predicts that the effects of insectivorous birds on insect herbivory on seedlings are greater beneath non-congeneric canopy trees. Although bird species richness and abundance were greater in broadleaved woodlands, birds were unable to regulate insect herbivory on seedlings in forests of more closely related tree species.